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Aquat. Living Resour.

14 (2001) 239−249
© 2001 Ifremer/CNRS/Inra/IRD/Cemagref/Éditions scientifiques et médicales Elsevier SAS. All rights reserved
S0990744001011238/FLA

Quality of Moroccan Atlantic coastal waters:


water monitoring and mussel watching
Abdelghani Chafika, Mohamed Cheggourb, Daniel Cossac*,
Samir Benbrahim Mostafa Sifeddinea
a
U.R.D. chimie marine, Institut national de recherche halieutique (INRH), 2, rue Tiznit, Casablanca, Morocco
b
Unité d’écologie, Département de biologie, École normale supérieure, B.P. 2400, Marrakech, Morocco
c
Ifremer, Centre de Nantes, B.P. 21105, 44311 Nantes cedex 3, France
Received 29 January 2001; accepted 25 April 2001

Abstract − The quality of Moroccan Atlantic coastal wasters was monitored from 1993 to 1997 by measuring hydrological
parameters (dissolved oxygen, suspended particulate matter, phosphates, and nitrates), and using the mussel Mytilus
galloprovincialis as a quantitative bioindicator of cadmium, copper, manganese, and zinc contamination. Mean concentrations of
dissolved oxygen and suspended particulate matter were indicative of the effects of urban and industrial discharges of wastewater,
particularly at Mohammedia, Casablanca, Mehdiya, Jorf Lasfar and Safi. Stations receiving urban wastewater showed high nitrate
concentrations, especially at Mehdiya, Rabat, Mohammedia, Casablanca and El Jadida. Metal concentrations in mussels showed
significant variations depending on the station and sampling period. Jorf Lasfar and Safi had the highest mean concentrations for
cadmium (8 and 7 µg·g–1 dry weight respectively) and copper (74 and 25 µg·g–1 dry weight). The relation between cadmium
concentrations in mussels, and phosphate concentrations in water suggests that the processing of phosphate ores at these two sites
is responsible for contamination. Mussels in the Mohammedia–Casablanca sector had the highest zinc concentrations
(338–379 µg·g–1 dry weight), followed by those collected at Jorf Lasfar (267 µg·g–1 dry weight), and Sidi Moussa and Safi
(290–301 µg·g–1 dry weight). The distribution of manganese concentrations, which were maximal in estuaries (up to 19 µg·g–1 dry
weight), was indicative of terrigenous inputs. Seasonal variations in mussel metal concentrations were characterised by winter
minima, and apparently related to the physiological cycle of the animal. With the exception of cadmium-contaminated areas, the
quality of mussels on the Moroccan Atlantic coast is good with respect to food safety standards.
© 2001 Ifremer/CNRS/Inra/IRD/Cemagref/Éditions scientifiques et médicales Elsevier SAS
bioindicator / monitoring / mussel watch / nutrients salts / trace elements / water quality

Résumé − Qualité physicochimique des eaux côtières et bioaccumulation métallique chez la moule Mytilus galloprovincialis
sur le littoral atlantique marocain. La qualité des eaux côtières atlantiques marocaines a été suivie de 1993 à 1996 par la mesure
des paramètres hydrologiques (oxygène dissous, matière en suspension, phosphates et nitrates) et l’utilisation de la moule (Mytilus
galloprovincialis) comme bioindicateur quantitatif de la contamination par le cadmium, le cuivre, le manganèse et le zinc. Les
teneurs moyennes en oxygène dissous et matière en suspension révèlent la trace des émissaires d’eaux usées urbaines et industrielles,
notamment à Mohammedia, Casablanca, Mehdiya, Jorf Lasfar et Safi. Les stations recevant des eaux usées urbaines, accusent
d’importantes teneurs en nitrates, en particulier au niveau de Mehdiya, Rabat, Mohammedia, Casablanca et El Jadida. Les teneurs
métalliques chez la moule montrent des variations significatives selon les stations et la saison de prélèvement. Les sites de Jorf Lasfar
et Safi, avec des concentrations moyennes respectivement de 8 et de 7 µg·g–1 (poids sec) en Cd, et de 74 et de 25 µg·g–1 (poids sec)
en Cu, se distinguent des autres stations. La relation entre les concentrations en Cd dans les moules et les concentrations en
phosphate dans les eaux suggère que le traitement des minerais de phosphates présent dans ces deux sites est à l’origine de cette
contamination. Ce sont les moules de Mohammedia–Casablanca qui sont les plus chargées en Zn (338–379 µg·g–1, poids sec), puis
celles collectées à Jorf Lasfar (267 µg·g–1, poids sec), Sidi Moussa et Safi (290–301 µg·g–1, poids sec). La distribution des concen-
trations en Mn, montre des maxima dans les estuaires (jusqu’à 19 µg·g–1, poids sec), et trace les apports terrigènes. Les variations
saisonnières des métaux chez la moule, caractérisées par des minima hivernales, semblent être liées au cycle physiologique de
l’animal. Du point de vue sanitaire, à l’exception des zones contaminées par le Cd, la qualité des moules du littoral atlantique
marocain est bonne. © 2001 Ifremer/CNRS/Inra/IRD/Cemagref/Éditions scientifiques et médicales Elsevier SAS
bioindicateur / suivi / monitorage quantitatif / sel nutritif / elément-trace / qualité de l’eau

*Correspondence and reprints: fax: +33 240 374 075.


E-mail address: dcossa@ifremer.fr (D. Cossa).
240 A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249

1. INTRODUCTION ‘African’ and a ‘Pacific’ coast (Bayed, 1982). The


African type consists of large beaches, estuaries, and
The Moroccan coast, like many other coastal re- high or low cliffs that alternate along the coast. The
gions in the world, is developing rapidly with respect Pacific type is characterised by old dunes, whose crests
to the socio-economic interests of the country. Demo- and sandstone ridges run parallel to the coast (Bayed,
graphic expansion, and continual urban and industrial 1982).
development are exposing coastal waters to increasing
contaminant discharges that convey various chemicals, 2.2. Socio-economic activities
including metals, into the sea. and contamination sources
The main purpose of this study was to evaluate the
physicochemical quality of the environment and the The Atlantic Larache–Safi area (figure 1) is the most
state of metal pollution in an area of relatively intense important one in Morocco because of a high popula-
human activity. It was performed during several an- tion and intensive industrial development. In fact, the
nual cycles (1993 to 1997) along a coastal area Atlantic coastal belt contains 61% of the Moroccan
running from the town of Larache on the North population, with maximum urban density along the
Atlantic seaboard, to Safi in the centre, a distance of Kénitra–Safi area (Kaioua, 1991). The towns use the
nearly 400 km. This assessment involved hydrological sea for final disposal of untreated wastewater, which
studies and analysis of certain metals in tissues of the contains a large and varied contaminant load. In 1990,
mussel Mytilus galloprovincialis, selected as a bioin- the amount of wastewater evacuated by coastal urban
dicator of the degree and extent of chemical pollution. areas along the area was estimated at 370 × 106 m3,
This work can thus be considered in part as a Moroc- and this figure may be expected to reach around
can ‘mussel watch’. Mussels are used worldwide as a 109 m3 within 30 years (Kaimoussi, 1996). According
bioindicator in monitoring programmes (e.g., Anon., to Benchekroun and Bouchama (1991), urban dis-
1980; Cossa, 1989; Stronkhorst, 1992; Cantillo, 1998). charges from Moroccan coastal towns constitute 55%
Moreover, various ecotoxicological studies have been of the total amount. The rapid demographic growth
concerned with mussels, which are frequently con-
sumed by man, and play an important role in the
transfer of chemical contaminants along food chains.
One of the main environmental problems with toxic
metals is their capacity to accumulate in the tissues of
living organisms, particularly bivalve molluscs col-
lected for human consumption. The absorption of large
amounts of metal by edible species could ultimately be
harmful to man at the upper end of the food chain.

2. ENVIRONMENTAL SETTINGS

2.1. The Moroccan Atlantic coast


The Atlantic coast of Morocco is subject to inter-
mittent upwellings of waters generally rich in nutrients
and trace elements. This phenomenon is not constant
along the coast, except for the Cape Spartel and the El
Jadida–Safi sectors. The tide is semidiurnal, with
variable amplitude (2.1 to 3.4 m). However, the tidal
currents have been rarely studied. The Canaries Cur-
rent, dominant at the surface, runs northeast to south-
west at a rate of 0.5 to 9 m.s–1, reaching its maximum
force in the 20–50 m stratum. The direction of this
current differs according to season (Fedoseev, 1970).
The swell is always fairly heavy, with maxima of up to
9 m, and associated currents can disperse pollutant
loads, ensuring their dissipation.
The Moroccan Atlantic coast is roughly straight.
The dominant landscape along the coast consists of
Figure 1. Location of coastal stations along the Moroccan Atlantic
sand dunes, more or less transformed into sandstone, coast between Larache and Safi. Lr: Larache, Mb: Moulay Bou
attaining 5 to 20 m in height and rarely covered by Selham, Md: Mehdiya (near Kénitra), Rb: Rabat, Mh1: Mohammedia
vegetation. Here and there, the coast is flat and rocky Station 1, Mh2: Mohammedia station 2, Cb: Casablanca, Db: Dar
without cliffs, or lined with low, moderately high Bouazza, Jd: El Jadida, Jl: Jorf Lasfar, Sm: Sidi Moussa, Ol: Oulidia,
cliffs. These elements are suggestive of both an Sf: Safi, and Sg: Souiria Guedima.
A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249 241

along the coastal belt has generally been accompanied 3.3. Analyses
by a high concentration of economic and industrial
activities. In fact, 80% of the industrial activities of
Morocco are concentrated along the Atlantic coast. In Seven physicochemical parameters were analysed in
1990, this area accounted for more than 75% of firms water. Temperature, total salinity (Model 33 YSI
and around 80% of jobs, mainly in the large cities. salinometer) and pH (ATC Piccolo HI 1280 pHmeter)
Seventy percent of the country’s companies can be were measured in situ. Dissolved oxygen was mea-
found between Kénitra and Safi, 85% of which exist in sured according to the protocol of Winkler adapted to
the administrative district of Casablanca. The domi- seawater. Suspended particulate matter (SPM) was
nant industries are of three main types: 1) metallurgi- estimated by differential weighing before and after
cal and electromechanical, 2) leather and textiles, and filtration (Whatman 0.7 µm) in a determined volume
3) chemical. Moreover, the Moroccan Atlantic sea- of water. Nitrate and phosphate analyses were per-
board concentrates 53% of tourism, and ensures 92% formed according to the methodology of Aminot and
of maritime transport. In addition to purely commer- Chaussepied (1983). Sampling bottles were rinsed in
cial transport, fishing activities are concentrated on the the laboratory with double distilled water and rinsed
Atlantic coast. again with the sampled water just before collection.
The Larache–Safi area includes four main plains After a period of purging in water from the sampling
with intensive farming activities, namely Loukkos, site, the mussels were transported to the laboratory in
Rharb, Doukkala and Abda, which all have direct a cooler at +4°C. The soft parts of mussels were
access to the Atlantic Ocean. This heavy agricultural removed from their shells, thoroughly cleaned and
development is associated with the use of increasing drained for 2 h according to the protocol described by
amounts of pesticides, fertilisers and other plant care Claisse (1989). They were then homogenised using a
products (biocides). According to several international grinder equipped with a stainless steel blade and
organisations, such as the UNEP (United Nations freeze–dried for conservation until analyses. A sub-
Environmental Program) and WHO (World Health sample of 1 g was homogenised in a porcelain mortar
Organisation), the exaggerated and uncontrolled use of before the mineralisation step. Mineralisation was
these substances can lead to chemical pollution, in- performed with 4 mL Suprapur nitric acid (Merck) in
cluding cadmium, mercury and copper. polyethylene tubes at room temperature for 12 h and
It is evident that each of these activities contributes then at 90°C for 3 h in a water bath. After cooling, the
directly or indirectly to the contamination of the digest was brought to 50 mL by addition of double
marine environment with various chemical substances, distilled water.
including metals. The present study investigated the
state of nutrient and metal contamination of the Metals (Cu, Cd, Zn, and Mn) were measured by
Moroccan Atlantic coast, using water analyses and the atomic absorption spectrophotometry (Perkin-Elmer,
mussel (Mytilus galloprovincialis) as a quantitative model 3100) equipped with a graphite furnace (HGA-
bioindicator. 600/700). The calculation of the coefficients of
variation for each metal analysis, based on reproduc-
ibility of replicates analyses on one sample, gave the
3. MATERIALS AND METHODS following relative coefficients of variation (i.e., stan-
dard deviation × 100 / average): Cu 11%; Cd 11%;
3.1. Study stations Mn 13%; Zn 8%, i.e. a mean reproducibility of about
90%. The accuracy of the method was tested using a
Fourteen coastal sites were chosen between Larache certified reference material obtained from the Interna-
and Safi (figure 1) in order to take into account the tional Atomic Energy Agency (CRM No. MA-A-
influences of natural and anthropogenic characteris- 2/TM). The error brackets obtained for the various
tics, namely, hydrographical influences (upwelling, metals analysed ranged from 7 to 9%. The detection
lagoons and estuaries) and urban, agricultural and limits were 0.004, 0.13, 0.05, and 4 µg·g–1 (dry
industrial discharges. Details are given in section 2.2. weight) for Cd, Cu, Mn, and Zn respectively.
3.2. Samples
Water and mussel samples were obtained at low tide 3.4. Statistical analysis
during the period 1993 to 1997. Water samples for
physicochemical analyses were collected in polyethyl-
ene flasks previously rinsed with distilled water. Statistical analysis performed with the Bioméco
Mussels were collected by hand at the mean low programme (Biométrie écologique) concerned mainly
water of neap tides on rocky substratum. Fifty adult the calculation of correlations between various param-
individuals (around 5 cm in size) were sorted on the eters. Analysis of variance (ANOVA) with Microsoft
field. They were then cleaned and stored in polyethyl- Excel software (version 7.0) allowed comparison of
ene flasks containing water from the sampling site and metal concentrations in mussel tissues relative to site
kept in a cooler (+4°C). and season.
242 A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249

Table I. Interannual means and standard deviations for hydrological parameters at marine stations along the Larache–Safi area.

Site Temperature Salinity pH Oxygen SPM Phosphate Nitrate


(°C) (g·kg–1) (mg·L–1) (mg·L–1) (µg·L–1) (µg·L–1)
Lr 19.1 ± 3.9 28.9 ± 2.4 7.9 ± 0.3 7.3 ± 0.8 41 ± 10 76 ± 37 84 ± 123
(13.5–24.9) (23.9–32.2) (7.3–8.2) (5.7–8.2) (21–60) (23–160) (23–480)
Mb 18.9 ± 3.9 31.2 ± 2.3 7.9 ± 0.3 8.0 ± 1.1 43 ± 10 117 +115 77 ± 68
(14–25) (28–35.2) (7.4–8.3) (6.5–9.0) (33–65) (30–470) (24–240)
Md 19.7 ± 4.0 29.4 ± 1.9 7.7 ± 0.3 6.2 ± 1.5 69 ± 34 268 +127 171 ± 262
(14–27) (26–32.9) (7.2–8.1) (2.76–8.0) (44–183) (107–527) (40–950)
Rb 19.6 ± 4.1 32.2 ± 1.4 7.8 ± 0.2 6.7 ± 1.6 34 ± 10 334 ± 213 181 ± 269
(15–26) (30–34.2) (7.3–8.0) (3.3–8.4) (20–50) (116–941) (41–980)
Mh1 18.7 ± 3.7 32.4 +2.3 8.0 ± 0.2 6.9 ± 0.7 27 ± 5 144 ± 159 41 ± 27
(13–24) (25–34.5) (7.4–8.3) (5.3–8.0) (19–35) (22–468) (23–100)
Mh2 19.1 ± 3.5 27.9 ± 2.4 7.5 ± 0.4 4.4 ± 2.1 58 ± 13 675 ± 446 187 ± 41
(14–24.5) (24.1–32) (6.8–8.0) (0.0–7.6) (42–86) (230–1858) (49–198)
Cb 19.8 ± 3.9 30.0 ± 1.5 7.4 ± 0.4 4.8 ± 1.4 60 ± 8 273 ± 105 325 ± 350
(15–25.5) (27.9–33) (6.6–8.0) (1.05–6.2) (47–76) (116–520) (57–1042)
Db 18.1 ± 2.9 32.6 ± 2.3 8.1 ± 0.2 8.0 ± 0.2 30 ± 9 92 ± 15 69 ± 29
(13.5–22) (28.3–35.8) (7.6–8.2) (7.4–9.5) (19–52) (76–129) (29–120)
Jd 17.1 ± 3.6 30.5 ± 2.1 7.9 ± 0.1 5.5 ± 0.4 40 ± 4 600 ± 53 263 ± 63
(11–24) (26.4–34) (7.8–8.1) (4.2–6.8) (31–46) (300–1500) (199–342)
Jl 19.5 ± 3.6 32.7 ± 1.4 7.7 ± 0.1 6.0 ± 0.7 65 ± 7 8910 ± 11 209 ± 101
(13.5–25.5) (28–35.2) (7.2–8.0) (5.0–7.8) (50–6) (640–19 830) (34–470)
Sm 18 ± 3.5 32.9 ± 1.5 7.9 ± 0.2 6.6 ± 0.9 35 ± 13 409 ± 382 130 ± 78
(12.7–22.5) (30.5–36) (7.5–8.1) (4.4–7.6) (15–53) (185–1710) (31–310)
Ol 17.3 ± 3.4 31.9 ± 1.8 7.9 ± 0.1 6.9 ± 0.8 36 ± 9 250 ± 120 171 ± 139
(11.5–21) (27.5–35) (7.8–8.1) (4.5–8.0) (20.5–49) (130–590) (51–581)
Sf 17 ± 3.15 33.5 ± 1.1 7.9 ± 0.1 6.3 ± 0.8 57 ± 6 4460 ± 514 108 ± 100
(12–21) (32–36) (7.7–8.1) (5.3–8.0) (49–67) (850–19 220) (24–440)
Sg 17.1 ± 2.9 33.0 ± 1.7 7.9 ± 0.2 6.9 ± 0.7 47 ± 6 850 ± 0.5 136 ± 121
(12–20.5) (27.9–35) (7.3–8.1) (5.7–7.7) (36–61) (290–1680) (36–440)

Values were calculated from 16 determinations between 1993 and 1997. In parentheses: range throughout the study period. SPM: suspended
particulate matter. Lr: Larache, Mb: Moulay Bou Selham, Md: Mehdiya (near Kénitra), Rb: Rabat, Mh1: Mohammedia Station 1, Mh2:
Mohammedia station 2, Cb: Casablanca, Db: Dar Bouazza, Jd: El Jadida, Jl: Jorf Lasfar, Sm: Sidi Moussa, Ol: Oulidia, Sf: Safi and Sg: Souiria
Guedima.

4. RESULTS The interannual means for dissolved oxygen in


water showed low levels in stations receiving un-
4.1. Hydrological parameters treated urban and industrial wastewater, particularly
Mohammedia, Casablanca, El Jadida, Jorf Lasfar and
The means for hydrological parameters, cumulated Safi. Hypoxia and even anoxia were observed at
throughout the study period (1993–1997), are given in Mohammedia and Casablanca (table I). The water at
table I. Water temperature showed slight seasonal the other stations appeared to be well oxygenated.
variations all along the Larache–Safi area. Variations Parallel to a decrease in the oxygenation rate of waters
of total salinity according to station were generally of from urban sites, suspended particulate matter (SPM)
low amplitude, although stations near river estuaries showed marked peaks, clearly indicating the input of
recorded a moderate decrease, notably at Larache, particles at Mohammedia, Casablanca, Mehdiya, Jorf
Mehdiya and Mohammedia (respectively near the Lasfar and Safi. Likewise, stations receiving urban
mouths of the Loukkos, oued Sebou and oued Mellah). wastewater showed high nitrate concentrations, espe-
These results indicate the extent of inputs from conti- cially at the level of Mehdiya, Rabat, Mohammedia,
nental waters into the ocean. A slight decrease in Casablanca and El Jadida (table I). The average
salinity was also observed at El Jadida and to a lesser concentrations at Oualidia, Sidi Moussa and Souiria
extent at Casablanca, apparently due to the large Guedima stations were fairly high, whereas those
quantity of effluents entering the sea near these sta- recorded at Larache and Moulay Bou Selham were in
tions. The mean pH values were close to 8, indicating the low range. Spatial variations in mean phosphate
the buffer effect of oceanic waters.
A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249 243

concentrations showed two marked peaks for Jorf Table III. F values for the analysis of variance (ANOVA) on metal
Lasfar (8.9 mg·L–1) and Safi (4.5 mg·L–1). The mean concentrations in the soft tissue of Mytilus galloprovincialis.
interannual concentrations at the other stations were
high, due essentially to urban discharges at Rabat and Factor Cu Cd Mn Zn
Mehdiya, urban and industrial discharges at Moham- Season 3.03*** 1.94* 10.12*** 6.35***
media, Casablanca and El Jadida, and agricultural Site 27.91** 54.66*** 19.41*** 11.67**
inputs at Moulay Bou Selham, Oualidia, Sidi Moussa
and Souiria Guedima. Results show that space (site) and time (season) discriminate
relatively to Cu, Cd, Mn and Zn concentrations. Asterisks refer to
4.2. Metal analyses in Mytilus galloprovincialis significance levels: * P < 0.05; ** P < 0.01; *** P < 0.001.

The mean metal concentrations cumulated through-


out the study period (1993–1997) are reported in table
II. The ANOVA on the basis of these concentrations 4.2.1. Spatial variations
(table III) showed significant variations according to Spatial variations in mean Cu concentrations were
station and sampling season. characterised by three clearly distinct peaks of variable
intensity at Jorf Lasfar and Safi (which showed higher
levels than other sites). Geographical variations in
Table II. Interannual means and standard deviations for metal con- mean Cd concentrations were quite close to those for
centrations in the mussel Mytilus galloprovincialis along the Larache-
Safi area.
Cu. The peaks at the Jorf Lasfar and Safi sites were
markedly above those of the other stations. The nature
Site Cu Cd Mn Zn of activities nearby (processing of phosphate ores)
suggests that inputs came from industrial and mining
Lr 10.6 ± 3.9 0.5 ± 1.0 12.5 ± 5.2 201 ± 113 operations. The lowest Cd levels were recorded at Dar
(5–18) (nd–0.9) (5.5–25.5) (175–533) Bouazza, followed very closely by those at Moulay
Mb 8.5 ± 3.5 0.4 ± 0.2 13.3 ± 4.4 117 ± 34 Bou Selham, Larache and north Mohammedia. Mus-
(4–15.8) (nd–0.7) (5.4–18.5) (72–184) sels from Mohammedia–Casablanca showed the high-
Md 10.4 ± 3.4 0.7 ± 0.3 19.1 ± 3.8 236 ± 72 est Zn concentrations, followed by those collected at
(6.9–19.6) (nd–1.9) (14.4–27.9) (84–325) Jorf Lasfar, Sidi Moussa, Safi and Souiria Guedima.
Rb 13.4 ± 4.5 0.6 ± 0.3 14.4 ± 4.3 256 ± 45 Similar levels were observed at Mehdiya and north
(8.1–23.1) (nd–1.5) (7.9–20.2) (186–317) Mohammedia, and lower levels at Moulay Bou Sel-
Mh1 6.9 ± 1.2 0.4 ± 0.3 9.6 ± 2.7 241 ± 94
ham and Dar Bouazza. The highest mean Mn concen-
(5.2–9.5) (nd–0.7) (6.1–16.1) (96–401) trations were observed at stations near estuaries and
lagoons, especially Mehdiya, Mohammedia-town, Ra-
Mh2 14.4 ± 3.9 1.1 ± 0.9 15.0 ± 2.8 338 ± 94
bat, Moulay Bou Selham and Sidi Moussa. However,
(10–24.2) (nd–2) (10.9–20) (265–645)
Mn concentrations were significant at Larache, the
Cb 18.1 ± 9.5 1.9 ± 1.0 8.8 ± 2.2 379 ± 66 entry to oued Loukkos, and Oualidia. These results
(9.5–40.1) (0.5–3) (5.9–13.2) (250–481) suggest that the sources of Mn are from riverine
Db 4.9 ± 1.2 0.2 ± 0.3 7.0 ± 1.6 152 ± 25 inputs.
(2.9–7) (nd–0.5) (5.2–10.3) (116–195)
Jd 6.7 ± 3.9 1.0 ± 0.8 6.3 ± 0.7 186 ± 142
4.2.2. Seasonal variations
(4–12.5) (0.1–2.9) (5.5–7) (110–398) The variations in seasonal metal concentrations in
Jl 73.5 ± 42.0 8 ± 5.9 7.4 ± 2.4 267 ± 70 tissues of the mussel M. galloprovincialis along the
(17–209) (3.5–15.5) (3.2–12.4) (189–456) Atlantic Larache–Safi area are indicated in figure 2,
Sm 12.0 ± 3.8 1.4 ± 1.1 13.0 ± 3.2 301 ± 151 with distinct bars for the means obtained for each
(5.6–16.7) (nd–2.5) (8.8–18.5) (85–545) season. The seasonal effect is testified by the results of
Ol 7.5 ± 2.6 0.9 ± 0.7 11.6 ± 4.5 202 ± 66
an analysis of variance (table III), which shows highly
(4.3–12) (nd–1.8) (6.3–20) (96–296) significant F coefficients for all metals studied. The
amplitude of the seasonal variations is usually less
Sf 24.7 ± 5.5 7 ± 3.8 8.5 ± 4.4 290 ± 59
than 20% but may reach a factor of 2. Mn and Zn
(12.5–39.7) (3.3–12.4) (3.7–17.1) (177–370)
concentrations for most stations were maximal in
Sg 7.9 ± 3.6 1.5 ± 1.9 8.3 ± 2 277 ± 80 spring and minimal in winter (figure 2). Though the
(4.6–18) (0.5–3.8) 7 (4–12.7) (67–371) minima for Cu and Cd were also observed in winter.
Values (in micrograms per gram, dry weight) were calculated from 16
determinations between 1993 and 1997. In brackets: minima and 5. DISCUSSION
maxima throughout the study period. nd: not detected (< detection
limit). Lr: Larache, Mb: Moulay Bousselham, Md: Mehdiya (near
Kénitra), Rb: Rabat, Mh1: Mohammedia Station 1, Mh2: Moham- 5.1. Quality of marine waters
media station 2, Cb: Casablanca, Db: Dar Bouazza, Jd: El Jadida, Jl:
Jorf Lasfar, Sm: Sidi Moussa, Ol: Oulidia, Sf: Safi and Sg: Souiria The spatiotemporal variations of various param-
Guedima. eters, notably nutrient salts, dissolved oxygen in water
244 A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249

Figure 2. Seasonal variations in metal concen-


trations in the mussel Mytilus galloprovincialis on
the Moroccan Atlantic coast between Larache and
Safi. Lr: Larache, Mb: Moulay Bousselham, Md:
Mehdiya (near Kénitra), Rb: Rabat, Mh1: Mo-
hammedia Station 1, Mh2: Mohammedia station
2, Cb: Casablanca, Db: Dar Bouazza, Jd: El
Jadida, Jl: Jorf Lasfar, Sm: Sidi Moussa, Ol:
Oulidia, Sf: Safi and Sg: Souiria Guedima. H:
winter, P: spring, E: summer, and A: autumn.

and SPM, are indicative of the quality of marine The concentrations of nutrients were within the
waters (Levitus et al., 1993; Fanning, 1992; Cheggour natural concentration range at Larache and Moulay
et al., 1999). Bou Selham in the north, and at Sidi Moussa and
In our study, water temperature differed little from Oualidia in the centre. However, their seasonal cycles
one site to another, whereas variations in total salinity (with high values in winter and low values in summer)
showed a significant decrease near river estuaries, were disturbed in urban centres such as Mohammedia–
indicating the presence of continental inputs, espe- Casablanca because of considerable human activity.
cially in the rainy season. The relatively marked drop Phosphate concentrations were particularly high at
in water temperature between El Jadida and Safi Jorf Lasfar and Safi, relative to phosphate-rich efflu-
showed that cold currents due to upwelling were ents from industrial complexes processing phosphates.
predominant in these areas. The large temperature rise These levels largely exceeded the means found for
recorded at Jorf Lasfar (19.5°C) can be attributed to surface waters of the Atlantic Ocean (Fanning, 1992;
the discharge of hot industrial wastewater from phos- Wiesenburg, 1988). High concentrations have also
phate processing complexes and a power plant. been reported for the Seine Bay (France), which drains
A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249 245

a heavily industrialised area, notably with phosphate 5.2. Metal contamination


processing plants (Anon., 1990). The average concen- of the mussel M. galloprovincialis
trations calculated for Oualidia and Sidi Moussa re-
flect agricultural practices in these two regions. The 5.2.1. Reasons for variations
nitrates used are recycled by tidal effects through in metal concentrations
lagoon systems before reaching the sea. The low The variations in metal concentrations in mussels
values recorded at Larache and Moulay Bou Selham depended on several parameters. Coastal environmen-
were due to low contaminant flux and high marine tal factors such as temperature and salinity (abiotic
dilution. The dilution seems more effective at Moulay factors) were taken into account as well as biological
Bou Selham because of the large size of the lagoon variables peculiar to the species, particularly those
(35 km2), which drains highly developed agricultural governing reproductive activity (biotic factors)
land in the region. This would account for the low (Mance, 1987; Cossa, 1989; Langston and Spence,
nitrate level found here compared to those of the 1995). In fact, it is difficult in a natural environment to
Oualidia and Sidi Moussa sites where adjacent lagoons sort the role played by each of these factors in the
are of much smaller size (6 and 7 km2). The nitrates overall assessment of bioconcentrations because of
detected near large cities suggest urban origin. How- their concomitant action.
ever, an industrial source was likely, especially at
Casablanca, relative to the activity of fertiliser plants 5.2.1.1. Abiotic factors
at Aïn Sebaa and Jorf Lasfar. The results for El Jadida The metal concentrations recorded along the
are consistent with the findings by Kaimoussi (1996), Larache–Safi area clearly showed that mussel popula-
who studied nitrate variations at stations receiving tions exposed to urban and industrial discharges were
urban sewages. These findings were confirmed by more contaminated with metal than those at some
SPM values, whose high peaks at urban sites were distance from these sources. High concentrations of
clearly indicative of an input of particles due to urban Cu, Zn and Cd are common in urban effluents (Guil-
effluents. The cases of Mohammedia, Casablanca, laud and Romana, 1991). In addition, Cd contamina-
Mehdiya, Jorf Lasfar and Safi constitute quite signifi- tion cases have been observed particularly in industrial
cant examples (table I). or agricultural discharges related to the exploitation,
processing or land disposal of phosphate minerals
(fertiliser and refuse) (Chiffoleau et al., 1994). The
Dissolved oxygen also showed low levels at these significantly negative correlations of these three met-
same sites. The values observed (table I) are consistent als with dissolved oxygen (RZn = –0.51, P < 0.05;
with the quantitative importance of the pollutant loads RCu = –0.53, P < 0.05; and RCd = –0.58, P < 0.01) tend
in effluents at the sites considered (Benbrahim et al., to confirm these hypotheses. Wastewater is a source of
1997). These discharges were rich in organic detritus metals and organic matter, which cause an impover-
whose bacterial oxidation reduced dissolved oxygen in ishment of dissolved oxygen. This heavy load has been
the environment. Nonetheless, in most of the sites the detected by analysis of effluents, notably at Casa-
levels observed did not appear to be critical for marine blanca (Benbrahim et al., 1997), El Jadida (Kaimoussi,
life because of the continual hydrodynamic mixing of 1996) and Rabat (Lemine, 1993).
coastal waters, which favours the dilution of the Significant positive correlations were found be-
organic matter load and allows rapid reoxygenation of tween phosphate and nitrate on the one hand and Cd
the water. The level of dissolved oxygen recorded at on the other (respectively, R = 0.61, P < 0.01; and
Mehdiya reflects the effect of inputs from the oued R = 0.57, P < 0.01), and between Cu and phosphates
Sebou, which conveys wastewater from the town of (R = 0.51, P < 0.05). These relationships support the
Kénitra and residues from port activities at both idea that Cd (and even Cu) inputs are of agricultural
Kénitra and Mehdiya. The values recorded at the origin, resulting from the leaching of cultivated fields
coastal stations of Oualidia and Sidi Moussa were previously enriched with fertilisers and products for
related to local organic inputs originating mainly in the plant treatments that contain metals. However, an
two lagoons and evacuated into the sea during their industrial origin is probably superimposed at Jorf
emptying at ebb tide. Lasfar and Safi, owing to discharges from chemical
complexes that process phosphates.
Manganese concentrations increased markedly after
Depending on the site, the results for pH indicated a the winter, in conjunction with rainfall maxima and an
greater or lesser enrichment of coastal waters with associated drop in salinity and temperature. The sig-
various forms of detritus emanating mainly from nificant negative correlations of Mn with salinity on
adjacent urban areas. This enrichment was significant the one hand (R = –0.61, P < 0.01) and temperature on
at stations receiving discharges of urban and/or indus- the other (R = –0.70, P < 0.01) suggest a crustal origin
trial wastewater either directly or via river estuaries. for this metal. Alternatively, these correlations may
This accounts for the ‘lower’ pH (compared to marine also indicate the influence of hydrological parameters
pH) at Mehdiya, Rabat, Casablanca, Safi and Jorf on the bioaccumulation of Mn within mussel tissues,
Lasfar. as already reported by Mance (1987).
246 A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249

5.2.1.2. Biotic factors tably at Oualidia and Sidi Moussa where this phenom-
Metal concentrations in mussel tissue showed sea- enon is nearly constant. Measurements of the Cd flux
sonal cycles, with minima in winter. Depending on the in upwelling zones of the Atlantic and Pacific Oceans
station, these cycles were more or less developed and have indicated a marked increase in this metal, com-
regular. This is in agreement with the results of pared to areas some distance away (e.g., Cossa and
Kaimoussi (1996) for the El Jadida region, where a Lassus, 1989).
marked spring peak was observed for several metals in Despite the magnitude of urban and industrial
soft tissues. In the Rabat–Mohammedia region, El liquid–solid discharges and inputs from agricultural
Hraiki (1992) reported significant variations of Cu and activities, which would seem to account for most of
Cd in the same mussel species and noted that concen- the Cd and Cu concentrations found in mussel tissues,
trations were maximal in the spring. Both authors atmospheric emissions cannot be entirely ruled out.
attributed these variations to the reproductive cycle of Although this factor has not been thoroughly studied,
the species. Moreover, Asso (1984), in a study of Nriagu and Pacyna (1988) estimated that worldwide
another bibalve (Perna perna) in the Bay of Algiers, atmospheric emissions of Cd from anthropogenic ac-
noted that several metals had an autumn maximum and tivities represent several thousand tons (between 3 and
a spring minimum, probably due to gametogenetic 12) per year, mainly from industrial sources. For the
phenomena. Winter maxima and high seasonal ampli- Western Mediterranean, Migon et al. (1991) estimated
tudes have been often observed in metal concentra- annual atmospheric fluxes (in thousands of tons) at
tions of Mytilus species from European coasts (e.g., 0.14 to 0.17 for Cd and 1.5 for Cu.
Claisse, 1989). This dissimilarity may be due to The Zn concentrations recorded in mussels indicate
differences in the biological cycle of the species (a the dominance of urban and industrial sources all
divergence in time and individual phasing) related to along the Larache–Safi area. Levels were particularly
latitudinal differences as a result of the various tem- high in the Mohammedia–Casablanca region where
perature cycles. wastewater discharge outlets are large. Mussels also
had relatively high Zn concentrations at the Rabat and
5.2.2. Origin and distribution of metals Mehdiya stations, which receive discharges from large
Phosphogypsum discharges from local chemical urban sewers as well as inputs from the Bou Regreg
complexes were responsible for much higher Cd and and Sebou estuaries respectively (figure 1).
Cu concentrations in mussels at Jorf Lasfar and Safi A crustal origin was more apparent for Mn. The
than at other coastal stations (Cheggour et al., 1999). tissue concentrations of this metal in mussels were
In fact, impurities rich in metals (notably Cu and Cd) quite elevated in stations close to the mouths of
have been frequently detected in phosphate concen- estuaries and lagoons and remarkably low in typical
trates produced in different regions of the world urban areas distant from these points. These results are
(Cossa and Lassus, 1989; Maxon and Vonkeman, in close agreement with other Moroccan studies indi-
1992). Not surprisingly, the concentrations of these cating that Mn is an excellent tracer of continental
metals in mussels were markedly lower at other inputs into aquatic systems produced by the breaking
Moroccan sites where this type of industry is not up of rocks and soils of surrounding watersheds
present, i.e. the Rabat region (El Hraiki, 1992) and (Carruesco, 1978; Texier et al., 1994).
north of Larache (Idrissi et al., 1994). However, the The present results for Morocco are concordant with
relatively high Cu and Cd levels found at Mohamme- those of other studies performed for areas along the
dia, Casablanca, Mehdiya and El Jadida are indicative Atlantic coast. For the El Jadida region, Kaimoussi
of the role of urban and industrial activities in gener- (1996) found high metal concentrations in surface
ating metal pollution. El Hraiki (1992) observed simi- sediments, algae and mussels sampled near urban and
lar Cd concentrations in mussels from the Mohamme- industrial wastewater sewers. Echab et al. (1996)
dia region, in agreement with reports for North observed high metal concentrations around effluents
Atlantic mussels (ICES, 1980). Cadmium concentra- from the town of Mohammedia, both in marine waters
tions recorded at sites ‘not primarily industrial’ were and mussels. The latter, collected on the Casablanca
generally lower, but still significant, as at Oualidia and coast, were heavily contaminated with metals, espe-
Sidi Moussa on the central Atlantic coast and to a cially at stations receiving wastewater (Cheggour et
lesser extent at Larache and Moulay Bou Selham on al., 1996). These results were confirmed by ecological
the north coast. These concentrations could relate to studies along the Casablanca coast, which showed a
the highly developed agricultural activities in these significant decrease in the diversity of intertidal mac-
regions, which use large amounts of fertiliser and plant robenthos near effluents of anthropogenic origin
care products. Although Cd and secondarily Cu are (Chafik et al., 1999). Physicochemical analyses of
minor constituents of these products, the large these effluents, performed regularly by the National
amounts used in intensive agriculture would contribute Institute of Halieutic Research (INRH) in Casablanca
to their accumulation in the environment and their showed high organic and unusually high metal con-
bioconcentration by organisms. It is also possible that centrations (Benbrahim et al., 1997). Similarly, our
the upwelling of waters rich in trace elements was a results at Safi are in complete agreement with those of
contributing factor (Bruland and Francks, 1983), no- Idrissi-Aatouf et al. (1996), who reported marked
A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249 247

contamination of mussels (and certain gastropods) in Table IV. Metal contamination indices (IcSx) for the mussel Mytilus
close relation to urban and industrial effluents. galloprovincialis along the Moroccan Atlantic coast between Larache
At an international level, the studies of Lauenstein and Safi.
and Dolvin (1992) conducted along American coasts
Site Cu Cd Mn Zn
reported significantly high metal concentrations in
M. edulis, which were attributed mainly to human Larache 0.68 0.24 1.12 0.81
activities. For the same species in the Baltic Sea, Moulay Bou Selham 0.54 0.11 1.20 0.48
Broman et al. (1991) observed relatively high Cd and Mehdiya 0.67 0.34 1.73 0.96
Zn levels, and described a north–south gradient deter- Rabat 0.85 0.21 1.30 1.04
mined by salinity variations as well as by anthropo- Mohammedia 1 0.44 0.20 0.87 0.98
Mohammedia 2 0.91 0.55 1.36 1.38
genic inputs into the marine environment. The moni-
Casablanca 1.15 0.98 0.80 1.54
toring of chemical contamination along French coasts Dar Bouazza 0.31 0.10 0.63 0.62
over a period of several years, using Mytilus sp. as a El Jadida 0.43 0.51 0.57 0.76
quantitative biological indicator, has allowed the iden- Jorf Lasfar 4.68 4.12 0.64 1.08
tification of certain ‘hot spots’ for anthropogenic Sidi Moussa 0.76 0.71 1.18 1.22
activity, characterised by particularly elevated levels Oualidia 0.48 0.50 1.05 0.82
of some metals such as Cd (Claisse, 1989). Safi 1.60 3.60 0.77 1.18
Souiria Guedima 0.50 0.80 0.75 1.13
5.2.3. Comparison of the stations
and the pollution gradient See text for definition of IcSx (section 5.2.3).
To compare metal pollution levels in mussels along
the Moroccan Atlantic coast, a metal contamination
index IcSx was calculated according to the equation: case, that of Larache–Safi area). According to the
results obtained (table IV), the following increasing
IcSx = Sx/M contamination gradient for all the metals combined
can be proposed: Dar Bouazza < (Oolidia, Sidi
where Sx is the mean concentration (in micrograms per Moussa) < (Moulay Bou Selham, Larache) < Souiria <
gram, dry weight) for metal x at station S, and M the Mohammedia (station 1) < El Jadida < (Mehdiya,
cumulative mean concentration (in micrograms per Rabat) < (Jorf Lasfar, Safi, Mohammedia (station 2,
gram, dry weight) for the same metal at all stations. In Casablanca).
the absence of any environmental standard, this index The comparison of the present metal data in mussels
allows the degree of contamination in different locali- with those of other localities in the world (table V)
ties to be compared with a regional average (in this indicates that the level of contamination on Moroccan

Table V. Range of metal concentrations in soft tissue of mussels from different localities in the world.

Locality Cu Cd Zn Reference
Larache–Casablanca, Morocco 6.6–14.4 0.4–1.9 117–379 Present studya
Jorf Lasfar–Safi, Morocco 24.7–73.5 7.0–8.0 267–290 Present studya
Rabat, Morocco 2.4–12.2 0.13–1.5 50–344 Chafai-El Alaoui (1994)a
Mohammedia, Morocco 13.6–16.8 0.8–0.93 – Echab et al. (1996)a
El Jadida, Morocco 4.4–14.7 nd–2.5 148–535 Kaimoussi (1996)a
Bay of Algiers, Algeria 10.8–15.7 0.54–1.8 133–243 Abada (1996)b
English Channel, France 3.8–16.5 0.4–8.8 53–318 Boutier (1982)c
Mediterranean, France 4.1–20.9 0.2–3.4 61–1336 Boutier (1982)a
Atlantic, France – 0.1–36.2 – Claisse (1989)c
Mediterranean, Italy 2.4–154 0.4–5.9 97–644 Abada (1996)a
Coast of Portugal 6.2–13.4 0.5–1.3 140–542 Coimbra et al. (1991)c
Atlantic, Spain 2–4 7–14 190–370 Manga (1980)c
South Devon, UK 0.2–17.3 0.8–36.2 16–634 Boalch et al. (1981)c
Baltic Sea – 5–11.5 121–160 Broman (1991)c
Coast of Sweden – 3.8 117 Broman (1991)c
Long Island, NY, USA 5.5–70 0.7–10 – Turgeon et al. (1989)c
USA coasts 5.7–530 0.9–9.1 67–6 000 Lauenstein et al. (1990)c
Pacific, USA 3.5–19.1 0.8–10.5 51–260 Goldberg et al. (1983)c
Pacific, Hong Kong 0.1–1.4 8.5–278 77–164 Phillips (1985)d
Victoria, Australia 3–11 2–140 126–747 Manga (1980)c
Derwent, Australia 24 42 352 Manga (1980)c

Values are in micrograms per gram, dry weight. (a) Mytilus galloprovincialis; (b) Perna perna; (c) Mytilus edulis; (d) Perna viridis; nd: not
detected.
248 A. Chafik et al. / Aquat. Living Resour. 14 (2001) 239–249

coasts is still moderate, except for a few sites. This Bayed, A., 1982. Écologie descriptive et dynamique des
justifies that current monitoring systems and pollution plages de la région de Rabat (Maroc), Ph.D. thesis.
control are necessary and should be reinforced. When Université de Bretagne Occidentale, Brest.
the results are considered in terms of the maximum Benbrahim, S., Chafik, A., Dafir, J., Zidane, F., 1997.
concentrations proposed by the Oslo and Paris Con- Contribution à l’étude de l’impact des rejets liquides sur
ventions and British guidelines for molluscs, the le littoral casablancais. Ressources halieutiques et envi-
quality of M. galloprovincialis relative to metal con- ronnement marin, Deuxièmes journées maghrébines des
tamination can be regarded as good at most stations on sciences de la mer, Agadir, Morocco.
the Moroccan Atlantic coast. However, Cd concentra- Benchekroun, M., Bouchama, M., 1991. La réutilisation des
tions at Jorf Lasfar and Safi are close to the current eaux usées en agriculture au Maroc. Gestion des ressour-
standards established by the European Community ces en eau, Septième congrès mondial, Rabat, Morocco.
regulation (No. 194/97). Boalch, R., Chan, S., Taylor, D., 1981. Seasonal variations in
the trace metal content of Mytilus edulis. Mar. Pollut.
Bull. 12, 276–280.
6. CONCLUSION
Boutier, B., 1982. Synthèse des résultats (RNO) de la
The water analyses along the Moroccan Atlantic surveillance des micropolluants dans la matière vivante.
Bulletin RNO Ifremer–ministère de l’Environnement,
coast between Larache and Safi showed some deterio-
vol. 17, pp. 115-174.
ration in quality (especially dissolved oxygen and
nutrients), at stations affected by heavy urban and Broman, D., Lindqvist, L., Lundbergh, I., 1991. Cadmium
industrial activities. This is the case for Mohammedia– and zinc in Mytilus edulis (L.) from the Bothnian sea and
Casablanca, Jorf Lasfar and Safi areas. Coastal waters the Northern Baltic. Proper. Environ. Pollut. 74, 227–244.
were of higher quality at sites with little or no human Bruland, K.W., Franks, R.P., 1983. Mn, Ni, Cu, Zn and Cd in
activity. the Western North Atlantic. In: Wong, C.S., Boyle, E.,
The Mussel Watch programme suggests a dominant Bruland, K.W., Burton, J.D., Goldberg, E.D. (Eds.), Trace
source of metal contamination from urban and indus- metals in sea water. Plenum Press, New York and London,
trial activities, and less important inputs from conti- pp. 395–414.
nental weathering and agricultural origins. Metal con- Carruesco, C., 1978. Comportement de quelques éléments
centrations distribution in mussels indicates hot spots métalliques dans les sédiments superficiels de la lagune
near large urban and industrial centres, notably Mo- de Moulay Bou Salham (côte atlantique marocaine). Bull.
hammedia–Casablanca. In addition, the mussels of Inst. Géol. Bassin d’Aquitaine 24, 37–48.
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Consequently, these sites need to be monitored quite Mussel Watch studies. Mar. Pollut. Bull. 39, 712–717.
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sources (e.g., Moulay Bou Selham, Sidi Moussa and contamination métallique chez certains mollusques et
Oualidia lagoons on the Atlantic coast), which have poissons marins: étude environnementale (côte atlantique
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